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CC BY 4.0 · Aorta (Stamford) 2018; 06(01): 001-012
DOI: 10.1055/s-0038-1639610
State-of-the-Art Review
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Epigenetics in Ascending Thoracic Aortic Aneurysm and Dissection

Adeline Boileau
1   Cardiovascular Research Unit, Luxembourg Institute of Health, Luxembourg, Luxembourg
,
Mark E. Lindsay
2   Department of Pediatrics, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
,
Jean-Baptiste Michel
3   UMRS 1148, INSERM, Paris 7-Denis Diderot University, Hôpital Xavier Bichat, Paris, France
,
Yvan Devaux
1   Cardiovascular Research Unit, Luxembourg Institute of Health, Luxembourg, Luxembourg
› Author Affiliations Funding A.B. is funded by the National Research Fund (grant # AFR 8832104). Y.D. is supported by the National Research Fund and the Ministry of Higher Education and Research of Luxembourg. M.E.L. is supported by the National Institutes of Health (grant #HL130113), and the Toomey Fund for Aortic Dissection Research. J.B.M. is funded by INSERM and Agence Nationale pour la Recherche GDPMs, NONAGES, and EU FP7: Fighting Aneurysmal Diseases.
Further Information

Publication History

Publication Date:
27 July 2018 (online)

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Abstract

Thoracic aortic aneurysm (TAA) is an asymptomatic and progressive dilatation of the thoracic aorta. Ascending aortic dissection (AAD) is an acute intraparietal tear, occurring or not on a pre-existing dilatation. AAD is a condition associated with a poor prognosis and a high mortality rate. TAA and AAD share common etiology as monogenic diseases linked to transforming growth factor β signaling pathway, extracellular matrix defect, or smooth muscle cell protein mutations. They feature a complex pathogenesis including loss of smooth muscle cells, altered phenotype, and extracellular matrix degradation in aortic media layer. A better knowledge of the mechanisms responsible for TAA progression and AAD occurrence is needed to improve healthcare, nowadays mainly consisting of aortic open surgery or endovascular replacement. Recent breakthrough discoveries allowed a deeper characterization of the mechanisms of gene regulation. Since alteration in gene expression has been linked to TAA and AAD, it is conceivable that a better knowledge of the causes of this alteration may lead to novel theranostic approaches. In this review article, the authors will focus on epigenetic regulation of gene expression, including the role of histone methylation and acetylation, deoxyribonucleic acid methylation, and noncoding ribonucleic acids in the pathogenesis of TAA and AAD. They will provide a translational perspective, presenting recent data that motivate the evaluation of the potential of epigenetics to diagnose TAA and prevent AAD.

Keywords

noncoding RNAs - histone acetylation - DNA methylation

On behalf of the Cardiolinc™ network (www.cardiolinc.org).


 

  • References

  • 1 Benjamin EJ, Blaha MJ, Chiuve SE. , et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart Disease and Stroke Statistics-2017 Update: a report from the American Heart Association. Circulation 2017; 135 (10) e146-e603
    CrossrefPubMedGoogle Scholar
  • 2 Bruneau BG. Epigenetic regulation of the cardiovascular system: introduction to a review series. Circ Res 2010; 107 (03) 324-326
    CrossrefPubMedGoogle Scholar
  • 3 Kim JB, Kim K, Lindsay ME. , et al. Risk of rupture or dissection in descending thoracic aortic aneurysm. Circulation 2015; 132 (17) 1620-1629
    CrossrefPubMedGoogle Scholar
  • 4 Jondeau G, Michel JB, Boileau C. The translational science of Marfan syndrome. Heart 2011; 97 (15) 1206-1214
    CrossrefPubMedGoogle Scholar
  • 5 Vapnik JS, Kim JB, Isselbacher EM. , et al. Characteristics and outcomes of ascending versus descending thoracic aortic aneurysms. Am J Cardiol 2016; 117 (10) 1683-1690
    CrossrefPubMedGoogle Scholar
  • 6 Michelena HI, Della Corte A, Prakash SK, Milewicz DM, Evangelista A, Enriquez-Sarano M. Bicuspid aortic valve aortopathy in adults: incidence, etiology, and clinical significance. Int J Cardiol 2015; 201: 400-407
    CrossrefPubMedGoogle Scholar
  • 7 Szabo Z, Crepeau MW, Mitchell AL. , et al. Aortic aneurysmal disease and cutis laxa caused by defects in the elastin gene. J Med Genet 2006; 43 (03) 255-258
    PubMedGoogle Scholar
  • 8 Superti-Furga A, Gugler E, Gitzelmann R, Steinmann B. Ehlers-Danlos syndrome type IV: a multi-exon deletion in one of the two COL3A1 alleles affecting structure, stability, and processing of type III procollagen. J Biol Chem 1988; 263 (13) 6226-6232
    PubMedGoogle Scholar
  • 9 Barbier M, Gross MS, Aubart M. , et al. MFAP5 loss-of-function mutations underscore the involvement of matrix alteration in the pathogenesis of familial thoracic aortic aneurysms and dissections. Am J Hum Genet 2014; 95 (06) 736-743
    CrossrefPubMedGoogle Scholar
  • 10 Magenis RE, Maslen CL, Smith L, Allen L, Sakai LY. Localization of the fibrillin (FBN) gene to chromosome 15, band q21.1. Genomics 1991; 11 (02) 346-351
    CrossrefPubMedGoogle Scholar
  • 11 Dasouki M, Markova D, Garola R. , et al. Compound heterozygous mutations in fibulin-4 causing neonatal lethal pulmonary artery occlusion, aortic aneurysm, arachnodactyly, and mild cutis laxa. Am J Med Genet A 2007; 143A (22) 2635-2641
    CrossrefPubMedGoogle Scholar
  • 12 Guo DC, Regalado ES, Gong L. , et al; University of Washington Center for Mendelian Genomics. LOX mutations predispose to thoracic aortic aneurysms and dissections. Circ Res 2016; 118 (06) 928-934
    CrossrefPubMedGoogle Scholar
  • 13 Zhu L, Vranckx R, Khau Van Kien P. , et al. Mutations in myosin heavy chain 11 cause a syndrome associating thoracic aortic aneurysm/aortic dissection and patent ductus arteriosus. Nat Genet 2006; 38 (03) 343-349
    CrossrefPubMedGoogle Scholar
  • 14 Guo DC, Pannu H, Tran-Fadulu V. , et al. Mutations in smooth muscle alpha-actin (ACTA2) lead to thoracic aortic aneurysms and dissections. Nat Genet 2007; 39 (12) 1488-1493
    CrossrefPubMedGoogle Scholar
  • 15 Guo DC, Regalado E, Casteel DE. , et al; GenTAC Registry Consortium; National Heart, Lung, and Blood Institute Grand Opportunity Exome Sequencing Project. Recurrent gain-of-function mutation in PRKG1 causes thoracic aortic aneurysms and acute aortic dissections. Am J Hum Genet 2013; 93 (02) 398-404
    CrossrefPubMedGoogle Scholar
  • 16 Loeys BL, Chen J, Neptune ER. , et al. A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat Genet 2005; 37 (03) 275-281
    CrossrefPubMedGoogle Scholar
  • 17 Lindsay ME, Schepers D, Bolar NA. , et al. Loss-of-function mutations in TGFB2 cause a syndromic presentation of thoracic aortic aneurysm. Nat Genet 2012; 44 (08) 922-927
    CrossrefPubMedGoogle Scholar
  • 18 Bertoli-Avella AM, Gillis E, Morisaki H. , et al. Mutations in a TGF-β ligand, TGFB3, cause syndromic aortic aneurysms and dissections. J Am Coll Cardiol 2015; 65 (13) 1324-1336
    CrossrefPubMedGoogle Scholar
  • 19 van de Laar IM, Oldenburg RA, Pals G. , et al. Mutations in SMAD3 cause a syndromic form of aortic aneurysms and dissections with early-onset osteoarthritis. Nat Genet 2011; 43 (02) 121-126
    CrossrefPubMedGoogle Scholar
  • 20 LeMaire SA, Russell L. Epidemiology of thoracic aortic dissection. Nat Rev Cardiol 2011; 8 (02) 103-113
    CrossrefPubMedGoogle Scholar
  • 21 Boileau C, Guo DC, Hanna N. , et al; National Heart, Lung, and Blood Institute (NHLBI) Go Exome Sequencing Project. TGFB2 mutations cause familial thoracic aortic aneurysms and dissections associated with mild systemic features of Marfan syndrome. Nat Genet 2012; 44 (08) 916-921
    CrossrefPubMedGoogle Scholar
  • 22 de Figueiredo Borges L, Martelli H, Fabre M, Touat Z, Jondeau G, Michel JB. Histopathology of an iliac aneurysm in a case of Menkes disease. Pediatr Dev Pathol 2010; 13 (03) 247-251
    CrossrefPubMedGoogle Scholar
  • 23 de Figueiredo Borges L, Jaldin RG, Dias RR, Stolf NA, Michel JB, Gutierrez PS. Collagen is reduced and disrupted in human aneurysms and dissections of ascending aorta. Hum Pathol 2008; 39 (03) 437-443
    CrossrefPubMedGoogle Scholar
  • 24 Bäck M, Gasser TC, Michel JB, Caligiuri G. Biomechanical factors in the biology of aortic wall and aortic valve diseases. Cardiovasc Res 2013; 99 (02) 232-241
    CrossrefPubMedGoogle Scholar
  • 25 Egger G, Liang G, Aparicio A, Jones PA. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004; 429 (6990): 457-463
    CrossrefPubMedGoogle Scholar
  • 26 Lee KK, Workman JL. Histone acetyltransferase complexes: one size doesn't fit all. Nat Rev Mol Cell Biol 2007; 8 (04) 284-295
    CrossrefPubMedGoogle Scholar
  • 27 Geiman TM, Robertson KD. Chromatin remodeling, histone modifications, and DNA methylation-how does it all fit together?. J Cell Biochem 2002; 87 (02) 117-125
    CrossrefPubMedGoogle Scholar
  • 28 Bestor TH. The DNA methyltransferases of mammals. Hum Mol Genet 2000; 9 (16) 2395-2402
    CrossrefPubMedGoogle Scholar
  • 29 Jin B, Li Y, Robertson KD. DNA methylation: superior or subordinate in the epigenetic hierarchy?. Genes Cancer 2011; 2 (06) 607-617
    CrossrefPubMedGoogle Scholar
  • 30 Devaux Y. Transcriptome of blood cells as a reservoir of cardiovascular biomarkers. Biochim Biophys Acta 2017; 1864 (01) 209-216
    CrossrefPubMedGoogle Scholar
  • 31 He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5 (07) 522-531
    CrossrefPubMedGoogle Scholar
  • 32 Goretti E, Wagner DR, Devaux Y. Regulation of endothelial progenitor cell function by micrornas. Minerva Cardioangiol 2013; 61 (06) 591-604
    PubMedGoogle Scholar
  • 33 Devaux Y, Zangrando J, Schroen B. , et al; Cardiolinc network. Long noncoding RNAs in cardiac development and ageing. Nat Rev Cardiol 2015; 12 (07) 415-425
    CrossrefPubMedGoogle Scholar
  • 34 Uchida S, Dimmeler S. Long noncoding RNAs in cardiovascular diseases. Circ Res 2015; 116 (04) 737-750
    CrossrefPubMedGoogle Scholar
  • 35 Engreitz JM, Pandya-Jones A, McDonel P. , et al. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 2013; 341 (6147): 1237973
    CrossrefPubMedGoogle Scholar
  • 36 Hansen TB, Jensen TI, Clausen BH. , et al. Natural RNA circles function as efficient microRNA sponges. Nature 2013; 495 (7441): 384-388
    CrossrefPubMedGoogle Scholar
  • 37 Guo G, Kang Q, Zhu X. , et al. A long noncoding RNA critically regulates Bcr-Abl-mediated cellular transformation by acting as a competitive endogenous RNA. Oncogene 2015; 34 (14) 1768-1779
    CrossrefPubMedGoogle Scholar
  • 38 Mitchell PS, Parkin RK, Kroh EM. , et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A 2008; 105 (30) 10513-10518
    CrossrefPubMedGoogle Scholar
  • 39 Goretti E, Wagner DR, Devaux Y. miRNAs as biomarkers of myocardial infarction: a step forward towards personalized medicine?. Trends Mol Med 2014; 20 (12) 716-725
    CrossrefPubMedGoogle Scholar
  • 40 Kumarswamy R, Bauters C, Volkmann I. , et al. Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circ Res 2014; 114 (10) 1569-1575
    CrossrefPubMedGoogle Scholar
  • 41 Vausort M, Wagner DR, Devaux Y. Long noncoding RNAs in patients with acute myocardial infarction. Circ Res 2014; 115 (07) 668-677
    CrossrefPubMedGoogle Scholar
  • 42 Devaux Y, Creemers EE, Boon RA. , et al; Cardiolinc network. Circular RNAs in heart failure. Eur J Heart Fail 2017; 19 (06) 701-709
    CrossrefPubMedGoogle Scholar
  • 43 Vausort M, Salgado-Somoza A, Zhang L. , et al. Myocardial infarction-associated circular RNA predicting left ventricular dysfunction. J Am Coll Cardiol 2016; 68 (11) 1247-1248
    CrossrefPubMedGoogle Scholar
  • 44 Lindsay ME, Dietz HC. Lessons on the pathogenesis of aneurysm from heritable conditions. Nature 2011; 473 (7347): 308-316
    CrossrefPubMedGoogle Scholar
  • 45 Gomez D, Al Haj Zen A, Borges LF. , et al. Syndromic and non-syndromic aneurysms of the human ascending aorta share activation of the Smad2 pathway. J Pathol 2009; 218 (01) 131-142
    CrossrefPubMedGoogle Scholar
  • 46 Borges LF, Gomez D, Quintana M. , et al. Fibrinolytic activity is associated with presence of cystic medial degeneration in aneurysms of the ascending aorta. Histopathology 2010; 57 (06) 917-932
    CrossrefPubMedGoogle Scholar
  • 47 Gomez D, Coyet A, Ollivier V. , et al. Epigenetic control of vascular smooth muscle cells in Marfan and non-Marfan thoracic aortic aneurysms. Cardiovasc Res 2011; 89 (02) 446-456
    CrossrefPubMedGoogle Scholar
  • 48 Gomez D, Kessler K, Michel JB, Vranckx R. Modifications of chromatin dynamics control Smad2 pathway activation in aneurysmal smooth muscle cells. Circ Res 2013; 113 (07) 881-890
    CrossrefPubMedGoogle Scholar
  • 49 Gomez D, Kessler K, Borges LF. , et al. Smad2-dependent protease nexin-1 overexpression differentiates chronic aneurysms from acute dissections of human ascending aorta. Arterioscler Thromb Vasc Biol 2013; 33 (09) 2222-2232
    CrossrefPubMedGoogle Scholar
  • 50 Shah AA, Gregory SG, Krupp D. , et al. Epigenetic profiling identifies novel genes for ascending aortic aneurysm formation with bicuspid aortic valves. Heart Surg Forum 2015; 18 (04) E134-E139
    CrossrefPubMedGoogle Scholar
  • 51 Liao M, Zou S, Weng J. , et al. A microRNA profile comparison between thoracic aortic dissection and normal thoracic aorta indicates the potential role of microRNAs in contributing to thoracic aortic dissection pathogenesis. J Vasc Surg 2011; 53 (05) 1341-1349.e3
    CrossrefPubMedGoogle Scholar
  • 52 Jones JA, Stroud RE, O'Quinn EC. , et al. Selective microRNA suppression in human thoracic aneurysms: relationship of miR-29a to aortic size and proteolytic induction. Circ Cardiovasc Genet 2011; 4 (06) 605-613
    CrossrefPubMedGoogle Scholar
  • 53 Patuzzo C, Pasquali A, Malerba G. , et al. A preliminary microRNA analysis of non syndromic thoracic aortic aneurysms. Balkan J Med Genet 2012; 15 (15, Suppl): 51-55
    PubMedGoogle Scholar
  • 54 Venkatesh P, Phillippi J, Chukkapalli S. , et al. Aneurysm-specific miR-221 and miR-146a participates in human thoracic and abdominal aortic aneurysms. Int J Mol Sci 2017; 18 (04) 184
    CrossrefPubMedGoogle Scholar
  • 55 Premakumari V, Chukkapalli S, Rivera M. , et al. Microrna expression signature in human thoracic and abdominal aortic aneurysms. Atherosclerosis 2014; 235 (02) e130
    PubMedGoogle Scholar
  • 56 Boon RA, Dimmeler S. MicroRNAs and aneurysm formation. Trends Cardiovasc Med 2011; 21 (06) 172-177
    CrossrefPubMedGoogle Scholar
  • 57 Boon RA, Seeger T, Heydt S. , et al. MicroRNA-29 in aortic dilation: implications for aneurysm formation. Circ Res 2011; 109 (10) 1115-1119
    CrossrefPubMedGoogle Scholar
  • 58 Merk DR, Chin JT, Dake BA. , et al. miR-29b participates in early aneurysm development in Marfan syndrome. Circ Res 2012; 110 (02) 312-324
    CrossrefPubMedGoogle Scholar
  • 59 Chen KC, Wang YS, Hu CY. , et al. OxLDL up-regulates microRNA-29b, leading to epigenetic modifications of MMP-2/MMP-9 genes: a novel mechanism for cardiovascular diseases. FASEB J 2011; 25 (05) 1718-1728
    CrossrefPubMedGoogle Scholar
  • 60 Mott JL, Kobayashi S, Bronk SF, Gores GJ. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 2007; 26 (42) 6133-6140
    CrossrefPubMedGoogle Scholar
  • 61 Cushing L, Costinean S, Xu W. , et al. Disruption of miR-29 leads to aberrant differentiation of smooth muscle cells selectively associated with distal lung vasculature. PLoS Genet 2015; 11 (05) e1005238
    CrossrefPubMedGoogle Scholar
  • 62 Deaton RA, Gan Q, Owens GK. Sp1-dependent activation of KLF4 is required for PDGF-BB-induced phenotypic modulation of smooth muscle. Am J Physiol Heart Circ Physiol 2009; 296 (04) H1027-H1037
    CrossrefPubMedGoogle Scholar
  • 63 van Rooij E, Sutherland LB, Thatcher JE. , et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 2008; 105 (35) 13027-13032
    CrossrefPubMedGoogle Scholar
  • 64 Du Y, Gao C, Liu Z. , et al. Upregulation of a disintegrin and metalloproteinase with thrombospondin motifs-7 by miR-29 repression mediates vascular smooth muscle calcification. Arterioscler Thromb Vasc Biol 2012; 32 (11) 2580-2588
    CrossrefPubMedGoogle Scholar
  • 65 Cordes KR, Sheehy NT, White MP. , et al. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009; 460 (7256): 705-710
    PubMedGoogle Scholar
  • 66 Pei H, Tian C, Sun X. , et al. Overexpression of microRNA-145 promotes ascending aortic aneurysm media remodeling through TGF-β1. Eur J Vasc Endovasc Surg 2015; 49 (01) 52-59
    PubMedGoogle Scholar
  • 67 Elia L, Quintavalle M, Zhang J. , et al. The knockout of miR-143 and -145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ 2009; 16 (12) 1590-1598
    CrossrefPubMedGoogle Scholar
  • 68 Cheng Y, Liu X, Yang J. , et al. MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ Res 2009; 105 (02) 158-166
    CrossrefPubMedGoogle Scholar
  • 69 Hergenreider E, Heydt S, Tréguer K. , et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 2012; 14 (03) 249-256
    CrossrefPubMedGoogle Scholar
  • 70 Chen J, Yin H, Jiang Y. , et al. Induction of microRNA-1 by myocardin in smooth muscle cells inhibits cell proliferation. Arterioscler Thromb Vasc Biol 2011; 31 (02) 368-375
    CrossrefPubMedGoogle Scholar
  • 71 Xie C, Huang H, Sun X. , et al. MicroRNA-1 regulates smooth muscle cell differentiation by repressing Kruppel-like factor 4. Stem Cells Dev 2011; 20 (02) 205-210
    CrossrefPubMedGoogle Scholar
  • 72 Torella D, Iaconetti C, Catalucci D. , et al. MicroRNA-133 controls vascular smooth muscle cell phenotypic switch in vitro and vascular remodeling in vivo. Circ Res 2011; 109 (08) 880-893
    CrossrefPubMedGoogle Scholar
  • 73 Li P, Zhu N, Yi B. , et al. MicroRNA-663 regulates human vascular smooth muscle cell phenotypic switch and vascular neointimal formation. Circ Res 2013; 113 (10) 1117-1127
    CrossrefPubMedGoogle Scholar
  • 74 Merlet E, Atassi F, Motiani RK. , et al. miR-424/322 regulates vascular smooth muscle cell phenotype and neointimal formation in the rat. Cardiovasc Res 2013; 98 (03) 458-468
    CrossrefPubMedGoogle Scholar
  • 75 Wang YS, Wang HY, Liao YC. , et al. MicroRNA-195 regulates vascular smooth muscle cell phenotype and prevents neointimal formation. Cardiovasc Res 2012; 95 (04) 517-526
    CrossrefPubMedGoogle Scholar
  • 76 Li P, Liu Y, Yi B. , et al. MicroRNA-638 is highly expressed in human vascular smooth muscle cells and inhibits PDGF-BB-induced cell proliferation and migration through targeting orphan nuclear receptor NOR1. Cardiovasc Res 2013; 99 (01) 185-193
    CrossrefPubMedGoogle Scholar
  • 77 Liu X, Cheng Y, Yang J, Xu L, Zhang C. Cell-specific effects of miR-221/222 in vessels: molecular mechanism and therapeutic application. J Mol Cell Cardiol 2012; 52 (01) 245-255
    CrossrefPubMedGoogle Scholar
  • 78 Leeper NJ, Raiesdana A, Kojima Y. , et al. MicroRNA-26a is a novel regulator of vascular smooth muscle cell function. J Cell Physiol 2011; 226 (04) 1035-1043
    CrossrefPubMedGoogle Scholar
  • 79 Dong S, Xiong W, Yuan J, Li J, Liu J, Xu X. MiRNA-146a regulates the maturation and differentiation of vascular smooth muscle cells by targeting NF-κB expression. Mol Med Rep 2013; 8 (02) 407-412
    CrossrefPubMedGoogle Scholar
  • 80 Zhang J, Zhao F, Yu X, Lu X, Zheng G. MicroRNA-155 modulates the proliferation of vascular smooth muscle cells by targeting endothelial nitric oxide synthase. Int J Mol Med 2015; 35 (06) 1708-1714
    CrossrefPubMedGoogle Scholar
  • 81 Liu X, Cheng Y, Chen X, Yang J, Xu L, Zhang C. MicroRNA-31 regulated by the extracellular regulated kinase is involved in vascular smooth muscle cell growth via large tumor suppressor homolog 2. J Biol Chem 2011; 286 (49) 42371-42380
    CrossrefPubMedGoogle Scholar
  • 82 Wang J, Yan CH, Li Y. , et al. MicroRNA-31 controls phenotypic modulation of human vascular smooth muscle cells by regulating its target gene cellular repressor of E1A-stimulated genes. Exp Cell Res 2013; 319 (08) 1165-1175
    CrossrefPubMedGoogle Scholar
  • 83 Li TJ, Chen YL, Gua CJ, Xue SJ, Ma SM, Li XD. MicroRNA 181b promotes vascular smooth muscle cells proliferation through activation of PI3K and MAPK pathways. Int J Clin Exp Pathol 2015; 8 (09) 10375-10384
    PubMedGoogle Scholar
  • 84 Davis BN, Hilyard AC, Lagna G, Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 2008; 454 (7200): 56-61
    CrossrefPubMedGoogle Scholar
  • 85 Ji R, Cheng Y, Yue J. , et al. MicroRNA expression signature and antisense-mediated depletion reveal an essential role of microRNA in vascular neointimal lesion formation. Circ Res 2007; 100 (11) 1579-1588
    CrossrefPubMedGoogle Scholar
  • 86 Yang J, Chen L, Ding J. , et al. MicroRNA-24 inhibits high glucose-induced vascular smooth muscle cell proliferation and migration by targeting HMGB1. Gene 2016; 586 (02) 268-273
    CrossrefPubMedGoogle Scholar
  • 87 Fiedler J, Stöhr A, Gupta SK. , et al. Functional microRNA library screening identifies the hypoxamir miR-24 as a potent regulator of smooth muscle cell proliferation and vascularization. Antioxid Redox Signal 2014; 21 (08) 1167-1176
    CrossrefPubMedGoogle Scholar
  • 88 Wanhainen A, Mani K, Vorkapic E. , et al. Screening of circulating microRNA biomarkers for prevalence of abdominal aortic aneurysm and aneurysm growth. Atherosclerosis 2017; 256: 82-88
    CrossrefPubMedGoogle Scholar
  • 89 Yu B, Liu L, Sun H, Chen Y. Long noncoding RNA AK056155 involved in the development of Loeys-Dietz syndrome through AKT/PI3K signaling pathway. Int J Clin Exp Pathol 2015; 8 (09) 10768-10775
    PubMedGoogle Scholar
  • 90 Zhao Y, Feng G, Wang Y, Yue Y, Zhao W. Regulation of apoptosis by long non-coding RNA HIF1A-AS1 in VSMCs: implications for TAA pathogenesis. Int J Clin Exp Pathol 2014; 7 (11) 7643-7652
    PubMedGoogle Scholar
  • 91 Wang S, Zhang X, Yuan Y. , et al. BRG1 expression is increased in thoracic aortic aneurysms and regulates proliferation and apoptosis of vascular smooth muscle cells through the long non-coding RNA HIF1A-AS1 in vitro. Eur J Cardiothorac Surg 2015; 47 (03) 439-446
    CrossrefPubMedGoogle Scholar
  • 92 Wang YN, Shan K, Yao MD. , et al. Long noncoding RNA-GAS5: a novel regulator of hypertension-induced vascular remodeling. Hypertension 2016; 68 (03) 736-748
    CrossrefPubMedGoogle Scholar
  • 93 Shan K, Jiang Q, Wang XQ. , et al. Role of long non-coding RNA-RNCR3 in atherosclerosis-related vascular dysfunction. Cell Death Dis 2016; 7 (06) e2248
    CrossrefPubMedGoogle Scholar
  • 94 Congrains A, Kamide K, Katsuya T. , et al. CVD-associated non-coding RNA, ANRIL, modulates expression of atherogenic pathways in VSMC. Biochem Biophys Res Commun 2012; 419 (04) 612-616
    CrossrefPubMedGoogle Scholar
  • 95 Liu W, Liu X, Luo M. , et al. dNK derived IFN-γ mediates VSMC migration and apoptosis via the induction of LncRNA MEG3: A role in uterovascular transformation. Placenta 2017; 50: 32-39
    CrossrefPubMedGoogle Scholar
  • 96 Lv J, Wang L, Zhang J. , et al. Long noncoding RNA H19-derived miR-675 aggravates restenosis by targeting PTEN. Biochem Biophys Res Commun 2017; S0006-291X(17)30011-6
    PubMedGoogle Scholar
  • 97 Wu G, Cai J, Han Y. , et al. LincRNA-p21 regulates neointima formation, vascular smooth muscle cell proliferation, apoptosis, and atherosclerosis by enhancing p53 activity. Circulation 2014; 130 (17) 1452-1465
    CrossrefPubMedGoogle Scholar
  • 98 Bell RD, Long X, Lin M. , et al. Identification and initial functional characterization of a human vascular cell-enriched long noncoding RNA. Arterioscler Thromb Vasc Biol 2014; 34 (06) 1249-1259
    CrossrefPubMedGoogle Scholar
  • 99 Ingber DE. Tensegrity II. How structural networks influence cellular information processing networks. J Cell Sci 2003; 116 (Pt 8, 116Pt 8): 1397-1408
    CrossrefPubMedGoogle Scholar
  • 100 Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009; 10 (01) 75-82
    CrossrefPubMedGoogle Scholar
  • 101 Isermann P, Lammerding J. Nuclear mechanics and mechanotransduction in health and disease. Curr Biol 2013; 23 (24) R1113-R1121
    CrossrefPubMedGoogle Scholar
  • 102 Sun SG, Zheng B, Han M. , et al. miR-146a and Krüppel-like factor 4 form a feedback loop to participate in vascular smooth muscle cell proliferation. EMBO Rep 2011; 12 (01) 56-62
    CrossrefPubMedGoogle Scholar
  • 103 Di Gregoli K, Mohamad Anuar NN, Bianco R. , et al. MicroRNA-181b controls atherosclerosis and aneurysms through regulation of TIMP-3 and elastin. Circ Res 2017; 120 (01) 49-65
    CrossrefPubMedGoogle Scholar
  • 104 Kee HJ, Kim GR, Cho SN. , et al. miR-18a-5p microRNA increases vascular smooth muscle cell differentiation by downregulating Syndecan4. Korean Circ J 2014; 44 (04) 255-263
    CrossrefPubMedGoogle Scholar
  • 105 Li J, Zhao L, He X, Yang T, Yang K. MiR-21 inhibits c-Ski signaling to promote the proliferation of rat vascular smooth muscle cells. Cell Signal 2014; 26 (04) 724-729
    CrossrefPubMedGoogle Scholar
  • 106 Yang G, Pei Y, Cao Q, Wang R. MicroRNA-21 represses human cystathionine gamma-lyase expression by targeting at specificity protein-1 in smooth muscle cells. J Cell Physiol 2012; 227 (09) 3192-3200
    CrossrefPubMedGoogle Scholar
  • 107 le Sage C, Nagel R, Egan DA. , et al. Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 2007; 26 (15) 3699-3708
    CrossrefPubMedGoogle Scholar
  • 108 Davis BN, Hilyard AC, Nguyen PH, Lagna G, Hata A. Induction of microRNA-221 by platelet-derived growth factor signaling is critical for modulation of vascular smooth muscle phenotype. J Biol Chem 2009; 284 (06) 3728-3738
    CrossrefPubMedGoogle Scholar
  • 109 Zhu XF, Shan Z, Ma JY. , et al. Investigating the role of the posttranscriptional gene regulator MiR-24- 3p in the proliferation, migration and apoptosis of human arterial smooth muscle cells in arteriosclerosis obliterans. Cell Physiol Biochem 2015; 36 (04) 1359-1370
    CrossrefPubMedGoogle Scholar